Macroevolution of Specificity in Cyanolichens of the GenusPeltigeraSectionPolydactylon(Lecanoromycetes, Ascomycota)

Abstract

Patterns of specificity among symbiotic partners are key to a comprehensive understanding of the evolution of symbiotic systems. Specificity of mutualistic partners, within a widespread monophyletic group for which all species are sampled has rarely been explored. Here, we assess the level of specificity between the cosmopolitan lichen-forming fungus (mycobiont) from the genus Peltigera, section Polydactylon, and its cyanobacterial partner Nostoc (cyanobiont). The mycobiont and cyanobiont phylogenies are inferred from five nuclear loci and the rbcLX region, respectively. These sequences were obtained from 206 lichen thalli, representing ca. 40 closely related Peltigera species sampled worldwide, doubling the number of known species in this group. We found a broad spectrum of specificity for both partners ranging from strict specialists to generalists. Overall, mycobionts are more specialized than cyanobionts by associating mostly with one or a few Nostoc phylogroups, whereas most cyanobionts associate frequently with several Peltigera species. Specialist mycobionts are older than generalists, supporting the hypothesis that specialization of mycobionts to one or few cyanobionts, is favored through time in geographic areas where species have been established for long periods of time. The relatively recent colonization of a new geographic area (Central and South America) by members of section Polydactylon is associated with a switch to a generalist pattern of association and an increased diversification rate by the fungal partner, suggesting that switches to generalism are rare events that are advantageous in new environments. We detected higher genetic diversity in generalist mycobionts. We also found that Peltigera species specialized on a single Nostoc phylogroup have narrower geographical distributions compared with generalist species.

Species diversification and phylogenetically constrained symbiont switching generated high modularity in the lichen genus Peltigera

“…This is totally plausible in our study system where some specific conditions/events seem to have primed the emergence of new modules and the diversification of Peltigera . For example, a Peltigera lineage within section Polydactylon colonized South America, which led to a switch to new cyanobiont phylogroups, selection towards generalism, a burst of speciation in this lineage, and the formation of a new module (module L, Figures and a; see also Magain, Miadlikowska, Goffinet, et al, ). In fact, fungal speciation and partner switching may not be independent from each other.…”

“…Because the phylogeny of Nostoc is incompletely resolved and poorly supported (Figure ; see also Magain, Miadlikowska, Goffinet, et al, ), we computed pairwise similarity distances as a proxy for phylogenetic distances among Nostoc phylogroups and distinct haplotypes. We assembled a dataset containing each of the 95 Nostoc groups (phylogroups and distinct haplotypes) represented in our interaction matrix, and computed pairwise distances corrected with the General Time Reversible (GTR) model, using PAUP v. 4.0a (Swofford, ).…”

“…We assembled a dataset of Peltigera-Nostoc interaction pairs summing up all information from the literature for which we could confidently assess the identity of the Peltigera species and Nostoc phylogroups or haplotypes (Chagnon et al, 2018;Lu et al, 2018;Magain, Miadlikowska, Goffinet, et al, 2017a;Magain, Miadlikowska, Mueller, et al, 2017b;Magain et al, 2018;Miadlikowska et al, 2014Miadlikowska et al, , 2018O'Brien, Miadlikowska, & Lutzoni, 2005;O'Brien, Miadlikowska, & Lutzoni, 2013;Pardo De la Hoz et al, 2018). The total dataset consisted of 1,026 thalli, or interaction pairs, representing 155 Peltigera species and 95 Nostoc phylogroups or haplotypes (Tables S1 and S2).…”

“…These lichenforming fungi (also referred to as mycobionts) are typically highly specialized on one or very few cyanobacterial phylogroup partners (also referred to as cyanobionts) that commonly associate with multiple Peltigera species (asymmetric specificity). The evolution of specialization has fuelled a large body of literature in ecology and evolution (Fisher, 1930;Levins, 1968;MacArthur, 1955;May, 1974) and one question that might be asked when looking at current patterns of specialization is whether selection towards such patterns was directional or stabilizing: in other words, is there a directional evolution towards specialization (Jaenike, 1990) or generalization (Waser, Chittka, Price, Williams, & Ollerton, 1996) or a combination of both, that is, specialization of Peltigera and generalization of Nostoc, which could be advantageous especially when symbionts are transmitted mostly horizontally (Chagnon et al, 2018;Lu et al, 2018;Lutzoni & Miadlikowska, 2009;Magain, Miadlikowska, Goffinet, Sérusiaux, & Lutzoni, 2017a)? Alternatively, has the specialization level of a guild been stable for a long time due to selection against higher, or lower, levels of specialization (i.e., stabilizing selection)?…”

Environment and host identity structure communities of green algal symbionts in lichens

“…Studies on symbiont diversity and community composition in lichens and other symbiotic associations have highlighted that fungal–algal community structure may not be predicted from niche properties and environment alone. Biotic factors, such as partner choice and population genetic processes of the host, may in fact play an important and, in some cases, even predominant role in determining the distribution of photobionts (Leavitt et al ., ; Magain et al ., ; Singh et al ., ). In accordance with this prediction, altitude was not the only driver of algal community assembly in our study.…”